Resolving marine–freshwater transitions by diatoms through a fog of discordant gene trees

Abstract

Despite the obstacles facing marine colonists, most lineages of aquatic organisms have colonized and diversified in freshwaters repeatedly. These transitions can trigger rapid morphological or physiological change and, on longer timescales, lead to increased rates of speciation. Diatoms are a lineage of ancestrally marine microalgae that have diversified throughout freshwater habitats worldwide. We generated a phylogenomic dataset of genomes and transcriptomes for 59 species to resolve freshwater transitions in one diatom lineage, the Thalassiosirales. Although most parts of the species tree were consistently resolved with strong support, we had difficulties resolving a Paleocene radiation, which affected the placement of one freshwater lineage. This and other parts of the tree were characterized by high levels of gene tree discordance caused by incomplete lineage sorting and low phylogenetic signal. Despite differences in species trees inferred from concatenation versus summary methods and codons versus amino acids, traditional methods of ancestral state reconstruction supported six transitions into freshwaters, two of which led to subsequent species diversification. However, simulations suggested as few as two independent transitions when accounting for hemiplasy, transitions occurring on branches in gene trees not shared with the species tree. This suggested that transitions across the salinity divide were originally facilitated by alleles already present in the ancestral marine populations. Accounting for differences in evolutionary outcomes, in which some taxa became locked into freshwaters while others were able to return to the ocean or become salinity generalists, might help distinguish between the ancestral changes that opened the door to freshwaters versus the subsequent, lineage-specific adaptations that allowed them to stay and thrive.

The dynamic response to hypo‐osmotic stress reveals distinct stages of freshwater acclimation by a euryhaline diatom

“…Diatoms, a diverse group of globally distributed microalgae that are abundant in habitats across the entire marine to freshwater salinity gradient, and across evolutionary timescales, transitions between marine and fresh waters have been an important source of species diversification (Nakov et al, 2018). Cyclotella cryptica is one of many euryhaline diatom species that occurs naturally in freshwater, brackish, and marine ecosystems (Cavalcante et al, 2013; Houk et al, 2010), and as part of an ancestrally freshwater clade (Roberts et al, 2022), is an important model for understanding the effects of salinity on diatom physiology. For example, salinity is known to impact the morphology of the siliceous cell wall of C. cryptica , including alterations to its thickness and ornamentation (Conley et al, 1989; Schultz, 1971).…”

Local adaptation of a marine diatom is governed by genome-wide changes in diverse metabolic processes

“…Although several of these pathways could be important for responses to other stressors, our data suggest that salinity is likely to be a major, though not sole, driver of local adaptation to the Baltic Sea. Finally, a phylogenomic study of Thalassiosirales, the diatom lineage to which S. marinoi belongs, identified 532 hemiplasious genes, i.e., ones with persistent ancestral polymorphisms associated with marine–freshwater transitions (62). A total of 151 of our outlier genes were also present in this set of hemiplasious genes, suggesting that the genes which contributed to ancient marine–freshwater transitions may have been similarly important for salinity adaptation over the microevolutionary timescales of this study.…”

CAnDI: a new tool to investigate conflict in homologous gene trees and explain convergent trait evolution

“…Examples include ancestral populations of butterflies that underwent introgressive hybridization to produce shared mimicry genes (Dasmahapatra et al 2012), incomplete or random lineage sorting resulting in unusually high levels of homoplasy in cacti (Copetti et al 2017), the distribution of karyotypic features in mammals (Robinson et al 2008), and the horizontal transfer of large DNA regions that explains the phylogenetic distribution of C4 photosynthesis in grasses (Dunning et al 2019). An adaptive role for genes in conflict was also established in tomato plants (Pease et al 2016), and more recently in Marsupials (Feng et al 2022) and Diatoms (Roberts et al 2023). Hence, investigating conflicting patterns can illuminate the evolution of complex traits and uncover molecular players that could contribute to novelty.…”